Impacts of gall induction on the structure and physiology of Caryocar brasiliense Camb. (pequi) leaves
Palavras-chave:
Gall inductionResumo
Gall induction commonly causes macro and microscopical effects in host leaves, such as a reduction in area, a spacing of chlorophyllian tissue, and a decrease in photosynthetic capacity linked to alterations in the contents of photosyntethizing pigments, as well as distinct histochemical profiles. These aspects were evaluated on galls induced by Eurytoma sp. (Hymenoptera) on leaves of Caryocar brasiliense and revealed the topographic disposition of the reserve substances in the galled tissues. This disposition indicates an ideal microenvironment for the Eurytoma sp. development and corroborates Nyman’s (2000) proposal for the determination of tissue zones in galls. The outer cortex and its phenolics accumulation confer protection, while the carbohydrates accumulation in the inner cortex fits for nutrition. Unexpectedly, the levels of infestation positively affect the host leaves by increasing their potential photosynthetic area. Also, photosynthetizyng pigments may guarantee basal levels of photosynthesis and accessory pigments, such as the carotenoids, may play the crucial antioxidant role in the gall chemical battle.
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Referências
Abrahamson, W.G., Mccrea, K.D., Whitwell, A.J., Vernieri, L.A. (1991). The
role of phenolics in goldenrold ball gall resistance and formation. Biochemical
Systematics and Ecology. 19 (8): 615-622. (novembro)
Barbosa, M.L.L., Acioli, A.N.S., Oliveira, A.N., Silva, N.M. Canto, S.L.O.
(2004). Ocorrência de Tuthillia cognata Hodkinson, Brown & Burckhardt,
1986 (Hemiptera: Homoptera, Psyllidae) em plantios experimentais de camucamu
Myrciaria dubia (H.B.K.) Mc Vaugh em Manaus (Amazonas, Brasil) Acta
Amazônica. 34 (1): 115-119.
Bronner, R. (1992). Biology of insect induced galls, in: Shorthouse, J.D. &
Rohfritsch, O., eds.The role of nutritive cells in the nutrition of cynipids and cecidomyiids,
Oxford University, Oxford. p. 118-140. Brundett, M.C., Kendrick, B., Peterson,
C.A. (1991). Efficient lipid staining in plant material with Sudan Red 7B or Fluoral
Yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry. 66: 111-116.
Castro, A.C., Oliveira, D.C., Moreira, A.S.F.P., Lemos-Filho, J.P., Isaias,
R.M.S. (2012). Source-sink relationship and photosynthesis in the horn-shaped
gall and its host plant Copaifera langsdorffii Desf. (Fabaceae). South African
Journal of Botany 83: 121-126
Castro, A.C.R., Leite, G.L.D., Isaias, R.M.S. Morphological patterns of a
hymenopteran gall on the leaflets of Caryocar brasiliense Camb. (Caryocaraceae).
American Journal of Plant Sciences 3: 921-929.
Fernandes, G.W., Martins, R.P. (1985). Tumores de plantas: as galhas. Ciência
Hoje. 19: 58-62.
Ferreira, K.M., Oliva, M.A., Hernandez-Terrones, M.G. (2005).
Caracterização histoquímica da folha de pequi (Caryocar brasiliense Camb.). In:
Congresso Nacional de Botânica Curitiba. Resumos: 56, Curitiba: UFPR.
Formiga, A.T., Gonçalves, S.J.M.R., Soares, G.L.G., Isaias, R.M.S. (2009).
Relações entre o teor de fenólicos e o ciclo de galhas de Cecidomyiidae em
Aspidosperma spruceanum Muel. Acta Botânica Brasilica. Arg. (Apocynaceae).
23: 93-99.
Formiga, A.T., Soares, G.L.G., Isaias R.M.S. (2011). Responses of the host
plant tissue in Aspidosperma spruceanum Arg. (Apocynaceae). American Journal
of Plant Science. 2: 350-358.
Gonçalves, S.J.M.R., Isaias, R.M.S.; Vale, F.H.A., Fernandes, G.W. (2005).
Sexual dimorphism of Pseudotectococcus rolliniae Hodgson & Gonçalves
(Hemiptera Coccoidea Eriococcidae) influences gall morphology on Rollinia
laurifolia Schltdl. (Annonaceae). Tropical Zoology 18: 161-169.
Harbone, J., Williams, C.A. (2000). Advances in flavonoid research since
1992. Phytochemistry. 55: 481-504.
Hartley, S.E. (1998). The chemical composition of plant galls: are levels of
nutrients and secondary compounds controlled by the gall-former? Oecologia.113:
492-501.
Isaias, R.M.S., Oliveira, D.C. (2011). Gall Phenotypes Product of Plant
Cells Defensive Responses to the Inducers Attack. In: Mérillon, Jean Michel;
Ramawat, Kishan Gopal. (Org.) Plant Defence: Biological Control. 1ed. New York:
Springer, 12: 273-290.
Isaias, R.M.S., Oliveira, D.C., Carneiro, R.G.S. (2011). Role of Euphalerus
ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of
Lonchocarpus muehlbergianus (Fabaceae). Botany. 89: 581-592.
Jensen, W.A. (1962). Botanical histochemistry: principles and practice. San
Francisco: W.H. Freeman, 408 p.
Johansen, D.A. (1940). Plant microtechnique. New York: McGraw-Hill Book
Co. Inc, 523 p.
Kraus, J.E., Arduin, M. (1997). Manual básico de métodos em morfologia vegetal.
Seropédica: EDUR, 198 p.
Kraus, J.E., Solórzano Filho, J.A., Arduin, M., Isaias R.M.S. (1994). Respostas
morfogenéticas de plantas brasileiras a insetos galhadores In: Fortunato, R.;
Bacigalupo, Proceedings of the VI Congresso Latinoamericano de Botânica. Mar del Plata,
Argentina.
Kraus, J.E., Sugiura, H.C., Cutrupi, S. (1996). Morfologia e ontogenia
em galhas entomógenas de Guarea macrophylla subsp. tuberculata (Meliaceae)
Fitopatologia Brasileira, 21 (3): 349-356.
Kraus, J.E., Tanoue, M. (1999). Morpho-ontogenetic aspects of
entomogenous galls in roots of Cattleya guttata (Orchidaceae) Lindleyana 14 (4):
204-213.
Krause, G.H. (1988). Photoinhibition of photosynthesis. An evaluation of
damaging andprotective mechanisms. Physiologia Plantarum. 74: 313-349.
Larson, K. C. (1998). The impact of two gall-forming arthropods on the
photosynthetic rates of their hosts. Oecologia.115: 161-166.
Larson, K.C., Whitham, T.G. (1991). Manipulation of food resources by a
gall-forming aphid: the physiology of sink-source interations. Oecologia. 88: 15-21.
Lichtenthaler, H., Wellburn, A. (1983). Determinations of total carotenoids
and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society
Transactions. 11 (5): 591-592.
Mani, M.S. (1964). Ecology of plant galls. The Hague: Dr. Junk Publishers,
434p.
Marques, M.C.S. (2001). Estudo fitoquímico dos extratos de pequi (Caryocar
brasiliense Camb.). Dissertação (Mestrado em Agroquímica/Agrobioquímica) –
Universidade Federal de Lavras, Lavras, 91 p.
Motta, L.B., Kraus, J.E., Salatino, A., Salatino, M.L.F. (2005). Distribution
of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra.
Biochemical Systematics and Ecology. 33: 971-981.
Nürnberger, T., Scheel, D. (2001). Signal transmission in the plant immune
response. Trends in Plant Science. 6 (8): 372-379.
Nyman, T., Widmer, A., Roininen, H. (2000). Evolution of gall morphology
and host-plant relationships in willow-feeding sawflies (Hymenoptera:
Tenthredinidae). Evolution. 54: 526-33.
Oliveira, D.C., Christiano, J.C.S., Soares, G.L.G., Isaias, R.M.S. (2006).
Reações estruturais e químicas de defesa de Lonchocarous muehlbergianus
(Fabaceae) e ação do galhador Euphalerus ostreoides (Hemiptera, Psyllidae),
Revista Brasileira de Botânica (Impresso). 29:657-667.
Oliveira, D.C., Isaias, R.M.S. (2010a). Cytological and histochemical
gradients inducing by sucking galls of Aspidosperma australe Arg. Muel.
(Apocynaceae). Plant Science, 178: 350-358.
Oliveira, D.C., Magalhães, T.A., Carneiro, R.G.S., Alvin, M.N.A., Isaias,
R.M.S. (2010). Do Cecidomyiidae gall induced by Aspidosperma spruceanum
(Apocynaceae) fit the pre-stablished cytological and histochemical patterns?
Protoplasma. 242: 81-93.
Oliveira, D.C., Isaias, R.M.S. (2010b). Redifferentiation of leaflet tissues
during midrib gall development in Copaifera langsdorffii (Fabaceae). South African
Journal of Botany. 76: 239-248.
Oliveira, D.C., Isaias R.M.S., Moreira, A.S.F.P., Lemos-Filho, J.P. (2011). Is
the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf
photosynthesis? Plant Science. 80:489-495.
Potikha, T.S., Collins, C. C., Johnson, D. I., Delmer, D. P. & Levine, A. (1999).
The involvement of hydrogen peroxide in the differentiation of secondary walls
in cotton fibers. Plant Physiology.119: 849-858.
Raman, A. (1991). Cecidogenesis of leaf galls on Syzygium cumini (L.)
Skeels (Myrtaceae) induced by Trioza jambolanae Crawford (Homoptera:
Psylloidea). Journal of Natural History.25: 653-663.
Russo, R. (2006). Field guide to plant galls of California and other Western
States. Univ. California Press, 397p.
Sass, J.E. (1951). Botanical microtechnique, 2nd ed. Ames: Iowa State College
Press, 391p.
Stone, G.N., Schönrogge, K. (2003). The adaptative significance of insect
gall morphology. Trends in Ecology and Evolution. 18 (10): 512-522.
Thiele, A.; Krause, G.H.; Winter, K. (1998). In situ study of photoinhibition
of photosynthesis and xantophyll cycle activity in plants growing in natural gaps
of the tropical forest. Australian Journal of Plant Physiology, 25: 189-195.
Welter, S. C. (1989). Arthropod impact on plant gas exchange. In: Bernays
EA (ed) Insect-plant interactions, CRC, Boca Raton, Fla, 1: 135-150.150.
role of phenolics in goldenrold ball gall resistance and formation. Biochemical
Systematics and Ecology. 19 (8): 615-622. (novembro)
Barbosa, M.L.L., Acioli, A.N.S., Oliveira, A.N., Silva, N.M. Canto, S.L.O.
(2004). Ocorrência de Tuthillia cognata Hodkinson, Brown & Burckhardt,
1986 (Hemiptera: Homoptera, Psyllidae) em plantios experimentais de camucamu
Myrciaria dubia (H.B.K.) Mc Vaugh em Manaus (Amazonas, Brasil) Acta
Amazônica. 34 (1): 115-119.
Bronner, R. (1992). Biology of insect induced galls, in: Shorthouse, J.D. &
Rohfritsch, O., eds.The role of nutritive cells in the nutrition of cynipids and cecidomyiids,
Oxford University, Oxford. p. 118-140. Brundett, M.C., Kendrick, B., Peterson,
C.A. (1991). Efficient lipid staining in plant material with Sudan Red 7B or Fluoral
Yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry. 66: 111-116.
Castro, A.C., Oliveira, D.C., Moreira, A.S.F.P., Lemos-Filho, J.P., Isaias,
R.M.S. (2012). Source-sink relationship and photosynthesis in the horn-shaped
gall and its host plant Copaifera langsdorffii Desf. (Fabaceae). South African
Journal of Botany 83: 121-126
Castro, A.C.R., Leite, G.L.D., Isaias, R.M.S. Morphological patterns of a
hymenopteran gall on the leaflets of Caryocar brasiliense Camb. (Caryocaraceae).
American Journal of Plant Sciences 3: 921-929.
Fernandes, G.W., Martins, R.P. (1985). Tumores de plantas: as galhas. Ciência
Hoje. 19: 58-62.
Ferreira, K.M., Oliva, M.A., Hernandez-Terrones, M.G. (2005).
Caracterização histoquímica da folha de pequi (Caryocar brasiliense Camb.). In:
Congresso Nacional de Botânica Curitiba. Resumos: 56, Curitiba: UFPR.
Formiga, A.T., Gonçalves, S.J.M.R., Soares, G.L.G., Isaias, R.M.S. (2009).
Relações entre o teor de fenólicos e o ciclo de galhas de Cecidomyiidae em
Aspidosperma spruceanum Muel. Acta Botânica Brasilica. Arg. (Apocynaceae).
23: 93-99.
Formiga, A.T., Soares, G.L.G., Isaias R.M.S. (2011). Responses of the host
plant tissue in Aspidosperma spruceanum Arg. (Apocynaceae). American Journal
of Plant Science. 2: 350-358.
Gonçalves, S.J.M.R., Isaias, R.M.S.; Vale, F.H.A., Fernandes, G.W. (2005).
Sexual dimorphism of Pseudotectococcus rolliniae Hodgson & Gonçalves
(Hemiptera Coccoidea Eriococcidae) influences gall morphology on Rollinia
laurifolia Schltdl. (Annonaceae). Tropical Zoology 18: 161-169.
Harbone, J., Williams, C.A. (2000). Advances in flavonoid research since
1992. Phytochemistry. 55: 481-504.
Hartley, S.E. (1998). The chemical composition of plant galls: are levels of
nutrients and secondary compounds controlled by the gall-former? Oecologia.113:
492-501.
Isaias, R.M.S., Oliveira, D.C. (2011). Gall Phenotypes Product of Plant
Cells Defensive Responses to the Inducers Attack. In: Mérillon, Jean Michel;
Ramawat, Kishan Gopal. (Org.) Plant Defence: Biological Control. 1ed. New York:
Springer, 12: 273-290.
Isaias, R.M.S., Oliveira, D.C., Carneiro, R.G.S. (2011). Role of Euphalerus
ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of
Lonchocarpus muehlbergianus (Fabaceae). Botany. 89: 581-592.
Jensen, W.A. (1962). Botanical histochemistry: principles and practice. San
Francisco: W.H. Freeman, 408 p.
Johansen, D.A. (1940). Plant microtechnique. New York: McGraw-Hill Book
Co. Inc, 523 p.
Kraus, J.E., Arduin, M. (1997). Manual básico de métodos em morfologia vegetal.
Seropédica: EDUR, 198 p.
Kraus, J.E., Solórzano Filho, J.A., Arduin, M., Isaias R.M.S. (1994). Respostas
morfogenéticas de plantas brasileiras a insetos galhadores In: Fortunato, R.;
Bacigalupo, Proceedings of the VI Congresso Latinoamericano de Botânica. Mar del Plata,
Argentina.
Kraus, J.E., Sugiura, H.C., Cutrupi, S. (1996). Morfologia e ontogenia
em galhas entomógenas de Guarea macrophylla subsp. tuberculata (Meliaceae)
Fitopatologia Brasileira, 21 (3): 349-356.
Kraus, J.E., Tanoue, M. (1999). Morpho-ontogenetic aspects of
entomogenous galls in roots of Cattleya guttata (Orchidaceae) Lindleyana 14 (4):
204-213.
Krause, G.H. (1988). Photoinhibition of photosynthesis. An evaluation of
damaging andprotective mechanisms. Physiologia Plantarum. 74: 313-349.
Larson, K. C. (1998). The impact of two gall-forming arthropods on the
photosynthetic rates of their hosts. Oecologia.115: 161-166.
Larson, K.C., Whitham, T.G. (1991). Manipulation of food resources by a
gall-forming aphid: the physiology of sink-source interations. Oecologia. 88: 15-21.
Lichtenthaler, H., Wellburn, A. (1983). Determinations of total carotenoids
and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society
Transactions. 11 (5): 591-592.
Mani, M.S. (1964). Ecology of plant galls. The Hague: Dr. Junk Publishers,
434p.
Marques, M.C.S. (2001). Estudo fitoquímico dos extratos de pequi (Caryocar
brasiliense Camb.). Dissertação (Mestrado em Agroquímica/Agrobioquímica) –
Universidade Federal de Lavras, Lavras, 91 p.
Motta, L.B., Kraus, J.E., Salatino, A., Salatino, M.L.F. (2005). Distribution
of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra.
Biochemical Systematics and Ecology. 33: 971-981.
Nürnberger, T., Scheel, D. (2001). Signal transmission in the plant immune
response. Trends in Plant Science. 6 (8): 372-379.
Nyman, T., Widmer, A., Roininen, H. (2000). Evolution of gall morphology
and host-plant relationships in willow-feeding sawflies (Hymenoptera:
Tenthredinidae). Evolution. 54: 526-33.
Oliveira, D.C., Christiano, J.C.S., Soares, G.L.G., Isaias, R.M.S. (2006).
Reações estruturais e químicas de defesa de Lonchocarous muehlbergianus
(Fabaceae) e ação do galhador Euphalerus ostreoides (Hemiptera, Psyllidae),
Revista Brasileira de Botânica (Impresso). 29:657-667.
Oliveira, D.C., Isaias, R.M.S. (2010a). Cytological and histochemical
gradients inducing by sucking galls of Aspidosperma australe Arg. Muel.
(Apocynaceae). Plant Science, 178: 350-358.
Oliveira, D.C., Magalhães, T.A., Carneiro, R.G.S., Alvin, M.N.A., Isaias,
R.M.S. (2010). Do Cecidomyiidae gall induced by Aspidosperma spruceanum
(Apocynaceae) fit the pre-stablished cytological and histochemical patterns?
Protoplasma. 242: 81-93.
Oliveira, D.C., Isaias, R.M.S. (2010b). Redifferentiation of leaflet tissues
during midrib gall development in Copaifera langsdorffii (Fabaceae). South African
Journal of Botany. 76: 239-248.
Oliveira, D.C., Isaias R.M.S., Moreira, A.S.F.P., Lemos-Filho, J.P. (2011). Is
the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf
photosynthesis? Plant Science. 80:489-495.
Potikha, T.S., Collins, C. C., Johnson, D. I., Delmer, D. P. & Levine, A. (1999).
The involvement of hydrogen peroxide in the differentiation of secondary walls
in cotton fibers. Plant Physiology.119: 849-858.
Raman, A. (1991). Cecidogenesis of leaf galls on Syzygium cumini (L.)
Skeels (Myrtaceae) induced by Trioza jambolanae Crawford (Homoptera:
Psylloidea). Journal of Natural History.25: 653-663.
Russo, R. (2006). Field guide to plant galls of California and other Western
States. Univ. California Press, 397p.
Sass, J.E. (1951). Botanical microtechnique, 2nd ed. Ames: Iowa State College
Press, 391p.
Stone, G.N., Schönrogge, K. (2003). The adaptative significance of insect
gall morphology. Trends in Ecology and Evolution. 18 (10): 512-522.
Thiele, A.; Krause, G.H.; Winter, K. (1998). In situ study of photoinhibition
of photosynthesis and xantophyll cycle activity in plants growing in natural gaps
of the tropical forest. Australian Journal of Plant Physiology, 25: 189-195.
Welter, S. C. (1989). Arthropod impact on plant gas exchange. In: Bernays
EA (ed) Insect-plant interactions, CRC, Boca Raton, Fla, 1: 135-150.150.
